A Freedom of Coxiella Burnetii Infection Survey in European Bison (Bison Bonasus) in Poland

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A Freedom of Coxiella Burnetii Infection Survey in European Bison (Bison Bonasus) in Poland animals Communication A Freedom of Coxiella burnetii Infection Survey in European Bison (Bison bonasus) in Poland Michał K. Krzysiak 1,2,* , Martyna Puchalska 3, Wanda Olech 4 and Krzysztof Anusz 3 1 Białowieza˙ National Park, Park Pałacowy 11, 17-230 Białowieza,˙ Poland 2 Institute of Forest Sciences, Faculty of Civil Engineering and Environmental Sciences, Białystok University of Technology, Wiejska 45 E, 15-351 Białystok, Poland 3 Department of Food Hygiene and Public Health Protection, Institute of Veterinary Medicine, Warsaw University of Life Sciences—SGGW, Nowoursynowska 159, 02-776 Warsaw, Poland; [email protected] (M.P.); [email protected] (K.A.) 4 Department of Animal Genetics and Conservation, Institute of Animal Science, Warsaw University of Life Sciences—SGGW, Ciszewskiego 8, 02-786 Warsaw, Poland; [email protected] * Correspondence: [email protected] Simple Summary: Q fever is one of the important diseases transmissible from animals to humans. The source of infection can be numerous species of animals including mammals, birds, reptiles, amphibians as well as ticks. The role of wildlife in its epidemiology is poorly understood. Therefore, we examined 523 sera samples obtained from European bison for the presence of specific antibodies to assess whether infection occurs in this species and whether European bison may be an important source of infection in the natural environment as suggested by historical reports. The antibodies were found only in one free-living bull, while two other samples were doubtful. The results suggest the transmission of infection to the European bison was rather accidental and its role as an important Citation: Krzysiak, M.K.; Puchalska, source of infection nowadays is unlikely. M.; Olech, W.; Anusz, K. A Freedom of Coxiella burnetii Infection Survey Abstract: Q fever is an important zoonosis caused by the intracellular Gram-negative bacteria in European Bison (Bison bonasus) Coxiella burnetii. The source of infection are numerous species of mammals, birds, reptiles and in Poland. Animals 2021, 11, 651. amphibians, as well as ticks. The disease is widespread throughout Europe, but the role of wildlife https://doi.org/10.3390/ani11030651 in its epidemiology is poorly understood. The European bison (Bison bonasus) population has been growing European-wide quite dynamically over the last few years. The aim of this study Academic Editor: was to determine whether C. burnetii infection occurs in European bison and whether it can be David González-Barrio considered an important bacterial reservoir in the natural environment. Five hundred and twenty Received: 1 February 2021 three samples of European bison sera originating from 14 (out of the 26 existing) Polish populations Accepted: 24 February 2021 were examined for the presence of specific antibodies using an ID Screen Q Fever Indirect Multi- Published: 1 March 2021 species ELISA test. Only one (0.19%) serum sample was positive in ELISA, and two other samples were doubtful. The only seropositive animal found in this study was a free-living bull. It suggests Publisher’s Note: MDPI stays neutral possible transmission from domestic cattle by sharing pastures. The transmission of C. burnetii into with regard to jurisdictional claims in the European bison was rather accidental in the country and its role as an important wild reservoir published maps and institutional affil- is unlikely. Since no tests are available for wildlife ruminants there is a need for the adaptation of iations. the available tests. Keywords: Coxiella burnetii; Q fever; serology; epidemiology; wildlife; European bison Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article 1. Introduction distributed under the terms and Q fever is a widely distributed reproductive disease of ruminants caused by intra- conditions of the Creative Commons cellular bacteria Coxiella burnetii. The pathogen is commonly transmitted to humans Attribution (CC BY) license (https:// and remains an emerging concern for public health. The source of infection are numer- creativecommons.org/licenses/by/ ous species of mammals, birds, reptiles and amphibians. Ticks are important vectors of 4.0/). Animals 2021, 11, 651. https://doi.org/10.3390/ani11030651 https://www.mdpi.com/journal/animals Animals 2021, 11, 651 2 of 9 C. burnetii transmission; therefore, the climate changes observed in the recent decades may provoke the shift of those arthropods into new locations, increasing the risk of tick-borne infections to occur [1]. In humans, infection as a result of a tick bite is rare, while potential sources of infection may be dusty feces of infected ticks, or exposure to dust with dried secretions of the reproductive system spread by the wind up to a distance of 2 km. Free- living animals may be a reservoir and source of C. burnetii infection for both humans and domestic animals. Q fever is widely spread all over Europe, however the role of wildlife in its transmission is still poorly understood. Dairy cattle are considered the main reservoir in Poland with the animal-level and herd-level seroprevalence around 25% [2]. C. burnetii DNA was detected in 3% of wildlife tested in a survey in the north-west of the country, which included roe deer, red deer and wild boar [3]. In the same study, the presence of bacteria was also confirmed in the ticks Ixodes ricinus from the same area. Other reports also confirmed the infection in wild ruminants, rabbits, rodents, foxes and ticks associated with their sylvatic ecosystems [4,5]. Moreover, specific antibodies were found in wild ranging cervids and mouflon [6,7]. European bison are the largest herbivores in Europe. Their conservation strategies should also include the monitoring of zoonotic diseases as an element of the One Health concept. However, Q fever studies have been neglected for the last two decades. The first report on the occurrence of C. burnetii in European bison dates back to the nineteen-eighties, when the exposure of forty-seven free-ranging European bison was investigated from Borecka forest (54◦5018.09” N 21◦55021.467” E) in connection to a Q fever epidemic in local cattle herds. The presence of specific antibodies was then confirmed in 76% of animals by the microagglutination test and complement fixation test (CFT) [8]. Furthermore, earlier in 1980–1983, a natural foci of Q fever could have been located in the Białowieska forest (52◦4209.861” N 23◦5104.52” E) [9], where the conservation of the endangered species after their complete extinction from the wild was initiated. Additionally, transmission to humans was suspected as 10% of European bison caretakers from Białowieza˙ National Park (52◦4209.861” N 23◦5104.52” E) became infected [8]. Further studies excluded exposure of European bison to C. burnetii by serological testing in 122 European bison from Białowieska forest in years 1991–2001 [10,11]. The population of the species, which remains listed by the International Union for Conservation (IUCN) of Nature’s Red List of Threatened Species increases successfully thanks to many national and international projects, reaching already n total of over 8400 individuals. They are most often reared in the enclosures but wild European bison population with frequent contact with people and domestic animals significantly increases [12]. In 2019, 74% of European bison were free-living [12]. Taking into account abovementioned, the aim of this study was to determine whether C. burnetii infection occurs in the European bison and whether it can be considered an im- portant bacterial reservoir in the natural environment. 2. Materials and Methods 2.1. Study Design To calculate the representative number of European bison in each of the populations to substantiate a prevalence of 1.5% or below with the overall α error set to 0.05, the FreeCalc software of Epitools [13,14] was used. The mean population size was determined by Euro- pean bison Pedigree Books (2013–2018). The targeted population size number increased from 1196 animals in 2013 to 1478 in 2018 with the mean value of 1377 individuals [12]. Considering the design prevalence at 1%, test sensitivity and specificity of about 100% and desired type I and II errors at 0.05, the targeted sample size for the whole population tested was 267. However, for the smaller herds, all the animals or all the available samples were included in the study. The samples were collected during the monitoring of European bison health in the years 2011–2017 as a part of the scientific cooperation of National Veterinary Research Institute in Puławy (NVRI) with herd/population managers based on: the opinion of the Minister of the Environment of 27 October 2014 (ZOP/06-061/51/2014); the Decision of the General Di- Animals 2021, 11, 651 3 of 9 Animals 2021, 11, 651 3 of 9 General Director for Environmental Protection of December 31, 2014 (DZP- rectorWG.6401.06.23.2014.km.2); for Environmental Protection individual of 31 permits December of the 2014 Director (DZP-WG.6401.06.23.2014.km.2); of the Białowieża National individualPark of December permits of20, the 2013 Director (PN/061/22/2013) of the Białowie and za˙May National 15, 2017 Park (PN of/061/14/2017) 20 December and 2013 per- (PN/061/22/2013)mits of the Kobiór and Forest 15 MayDistrict 2017 (ZG (PN/061/14/2017)-7326 (1) -9/2014). and Since permits 2017, ofthe the sample Kobió collectionr Forest Districthas been (ZG-7326 carried (1) out -9/2014). as part of Since the 2017,project the “Complex sample collection project of has European been carried bison out conserva- as part oftion the by project State “Complex Forests” financed project of by European the Forest bison Fund conservation (Poland) in by accordance State Forests” wit financedh contract byNo. the OR.271.3.10.2017. Forest Fund (Poland) in accordance with contract No.
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